Synchronous inhibitory pathways create both efficiency and diversity in the retina

Visual information is conveyed from the retina to the brain by a diverse set of retinal ganglion cells. Although they have differing nonlinear properties, nearly all ganglion cell receptive fields on average compute a difference in intensity across space and time using a region known as the classical or linear surround a property that improves information transmission about natural visual scenes. The spatiotemporal visual features that create this fundamental property have not been quantitatively assigned to specific interneurons. Here we describe a generalizable causal approach using simultaneous intracellular and multielectrode recording to directly measure and manipulate the sensory feature conveyed by a neural pathway to a downstream neuron. Analyzing two inhibitory cell classes, horizontal cells and linear amacrine cells, we find that rather than transmitting different temporal features, the two inhibitory pathways act synchronously to create the salamander ganglion cell surround at different spatial scales. Using these measured visual features and theories of efficient coding, we computed a fitness landscape representing the information transmitted using different weightings of the two inhibitory pathways. This theoretical landscape revealed a ridge that maintains near-optimal information transmission while allowing for receptive field diversity. The ganglion cell population showed a striking match to this prediction, concentrating along this ridge across a wide range of positions using different weightings of amacrine or horizontal cell visual features. These results show how parallel neural pathways synthesize a sensory computation, and why this architecture achieves the potentially competing objectives of high information transmission of individual ganglion cells, and diversity among receptive fields.